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Two Kinds of Persistent Soil Seed Banks in an Amphi-Basicarpic Cold-Desert Annual

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Two Kinds of Persistent Soil Seed Banks in an Amphi-Basicarpic Cold-Desert Annual Seed Science Research (2014) 24, 293–300 doi:10.1017/S0960258514000270 q Cambridge University Press 2014 Two kinds of persistent soil seed banks in an amphi-basicarpic cold-desert annual Juan J. Lu1, Dun Y. Tan1*, Jerry M. Baskin1,2 and Carol C. Baskin1,2,3* 1Xinjiang Key Laboratory of Grassland Resources and Ecology and Ministry of Education Key Laboratory for Western Arid Region Grassland Resources and Ecology, College of Grassland and Environment Sciences, Xinjiang Agricultural University, Uru¨mqi 830052, China; 2Department of Biology, University of Kentucky, Lexington, KY 40506, USA; 3Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546, USA (Received 17 May 2014; accepted after revision 25 July 2014; first published online 3 September 2014) Abstract Introduction Several studies have compared seed banks of the Although many species of flowering plants produce different morphs of heteromorphic species, but none of fruits and seeds that vary continuously in size, mass them was on an amphi-basicarpic species. Our and various other traits, individuals of a few hundred primary aim was to compare the relative ability of species produce two or more kinds of diaspores that aerial and basal diaspores of an amphi-basicarpic exhibit distinct differences in morphology as well as in species to form a seed bank. We compared the seed- ecology (Harper, 1977; Manda´k, 1997; Imbert, 2002). bank dynamics of basal and aerial diaspores of three This latter phenomenon is known as fruit/seed populations of the cold-desert annual Ceratocarpus heteromorphism, and it is considered to be an arenarius growing in the Junggar Desert in north- adaptation of species to the spatio-temporal variability western China. A 2.5-year experimental garden study (unpredictability) of stressful habitats (Venable and compared germination phenology and retention of Lawlor, 1980; Venable, 1985). That is, if dispersal units viability in basal (a) and aerial (c and f) morphs. Aerial from the same plant differ in how they respond to the morphs formed a modified Thompson and Grime type environment, there is an increased chance that some of III seed bank (small proportion of seeds carried over to them will survive, germinate and produce new plants. next year) and the basal morph a modified type IV Baskin and Baskin (2014) recognized two general seed bank (large proportion of seeds carried over to categories of fruit/seed heteromorphism: heterodiasp- next year). Seeds germinated only in spring, and ory and amphicarpy. In heterodiaspory, two or more cumulative germination percentages were f . c . a morphs are produced above ground, and in amphi- (year 1), f ¼ c . a (year 2) and f ¼ c ¼ a (year 3). The carpy one or more morph(s) are produced above relationship between length of germination period, ground and one or more below ground. Heterodiasp- retention of viability during burial and relative ability to ory was divided further into four subcategories: form a persistent seed bank was basal morph . aerial heterocarpy, two or more types of fruits (sometimes morphs. The results of this seed-bank study on with accessory parts, such as perianth, bracteoles or C. arenarius are in full agreement with those published phyllary); heteroarthrocarpy, one type of fruit with previously on seed dispersal and dormancy in this distinct segments (i.e. proximal versus distal), each species. Thus, strong additional support is provided bearing a distinct seed morph; heterospermy, one or for a high risk–low risk germination strategy in this more types of fruits containing seeds that differ within cold-desert annual. and/or between fruits; and amphi-basicarpy, flowers and fruits produced at or near ground level and on Keywords: amphi-basicarpic annual, bet-hedging, aerial parts of the stem. Ceratocarpus, diaspore heteromorphism, retention of The ecology of heteromorphic fruits and seeds has diaspore viability, soil seed bank been studied extensively in heterocarpous (e.g. Baker and O’Dowd, 1982; Venable and Levin, 1985a, b; Venable et al., 1987; Imbert et al., 1996, 1999; Bra¨ndel, 2007), heteroarthrocarpous (e.g. Payne and Maun, *Correspondence 1981; Maun and Payne, 1989; Zhang and Maun, 1992; Email: [email protected] or [email protected] Donohue, 1998; Cordazzo, 2006), heterospermous 294 J.J. Lu et al. (e.g. Cronin, 1965; Wang et al., 2008; Lu et al., 2010; Yao Plants produce two basicarps (dispersal unit type a) et al., 2010) and amphicarpous (e.g. Weiss, 1980; near the soil surface and a gradient of aerial dispersal Cheplick and Quinn, 1982; Cheplick, 1994; Ruiz de types (b–f) in different canopy positions (Fig. 1A). The Clavijo and Jime´nez, 1998; Sadeh et al., 2009) species. total number of aerial dispersal units was 35–740, However, the only amphi-basicarpic species that we depending on the plant size. Thus, C. arenarius is an are aware of, for which the ecology of its hetero- amphi-basicarpic species (sensu Barker, 2005). When diaspores has been compared is the chenopod species mature, some aerial dispersal units are dispersed by Ceratocarpus arenarius L. (Amaranthaceae). In this wind before the stem breaks near the base, and others heteromorphic species, the aerial morphs have high become detached as plants tumble across the land- dispersal ability and a low degree of dormancy, and scape (Zhou, 2009; Lu et al., 2013). The two dispersal the basal morphs have low dispersal ability and a high units at the base of the plant remain attached to the degree of dormancy (Gao et al., 2008; Zhou, 2009; Lu rooted basal part of the dead plant after the stem et al., 2013). That is, the aerial morphs exhibit a high- breaks and are not dispersed. Flowering of C. arenarius risk strategy for dispersal and dormancy and the begins in late April and ends in September, dispersal/ basicarp morph a low-risk strategy (Baskin et al., 2014). germination units (fruits þ bracteoles) mature from Several studies have compared the ability of the late July to early October and seeds germinate in late different morphs of heteromorphic species to form March to mid-April. a soil seed bank. Most of these studies have been on The study on seed-bank dynamics was done in dimorphic species, and in the majority of cases one three natural populations of C. arenarius, each morph forms a transient seed bank and the other a consisting of several thousand plants growing on persistent seed bank (Robocker et al., 1969; Philipu- sand dunes in the vicinity of Fukang City on the pillai and Ungar, 1984; Ungar, 1984; Venable and Levin, southern edge of the Junggar Basin of Xinjiang 1985b; Wertis and Ungar, 1986; Carter and Ungar, 2003; Province, China (448090N, 878580E, 438 m above sea Cao et al., 2012). In the trimorphic species Atriplex level). The sand does not exhibit soil profile develop- sagittata, one morph forms a transient seed bank and ment, and it is low in organic matter. Mean annual the other two a persistent seed bank (Manda´k and temperature is 8.38C, and the mean temperatures of the Pysˇek, 2001). However, a few studies have reported coldest (January) and hottest (July) months are that both morphs formed a transient (Venable et al., 215.68C and 26.08C, respectively. Average annual 1987) or a persistent (Callihan et al., 1993; Joley et al., precipitation (including rain and snow) is 222 mm, 2003) soil seed bank. about two-thirds of which falls in spring and summer, Heretofore, the relative ability of aerial and basal and the snow that falls in winter begins to melt in diaspore morphs of amphi-basicarpic species to form March or April (data from Fukang weather station, a seed bank has not been reported. The purpose of our 2001–2010). Annual potential evaporation is study was to compare the seed-bank dynamics of aerial .2000 mm (Wei et al., 2003). and basicarpic diaspores of the amphi-basicarpic Among other species, the flora/vegetation of annual C. arenarius. Based on the high-risk strategy of sand dunes in the southern part of the Junggar the aerial morphs of this species for dispersal and Basin consists of the dwarf tree Haloxylon persicum dormancy (see below) and the low-risk strategy for the basicarps (see below), we hypothesized that the basicarp morph had a greater ability to form a persistent seed bank than the aerial morphs. To test this hypothesis, we compared seed-bank dynamics, germi- nation phenology and retention of seed viability during burial of aerial and basicarpic morphs of C. arenarius. Materials and methods Study species, field site and dispersal unit collection Ceratocarpus arenarius is a summer annual species that Figure 1. (colour online) (A) Spatial position of basicarpic occurs in middle and central Asia (including north- (a) and aerial (b–f) dispersal units of Ceratocarpus arenarius west China) (Mao, 1994). In China, the species is found on an individual plant, and (B) morphology of the six types only in the cold deserts of northern Xinjiang Province. of dispersal units of C. arenarius. The stem of this tumble- The fruit, with two permanently attached bracteoles, is weed breaks at the node that is labelled. Circled material the dispersal and germination unit of this species. from (www.chinabaike.com). gl, glochid. Soil seed bank in an amphi-basicarpic annual 295 (Amaranthaceae); the shrub Calligonum leucocladum (experimental garden) conditions. Three replicates (Polygonaceae); the dwarf subshrub Artemisia arenaria of 200 dispersal units of each of the three morphs (Asteraceae); the perennial herbs Allium and Astragalus collected on 6 October 2010 were sown to a depth of species; various species of summer annual chenopods c. 0.5 cm in plastic pots (18 cm deep and 21 cm in (Amaranthaceae), e.g. Agriophyllum squarrosum and diameter with drainage holes at the bottom) filled C.
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